A NEW SPECIES OF RARICIRRUS (POLYCHAETA, CTENODRILIDAE) FROM THE CONTINENTAL SLOPE OF THE LAPTEV SEA NEAR THE GAKKEL RIDGE
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1 Proceedings of the Zoological Institute RAS Vol. 321, No. 4, 2017, рр УДК A NEW SPECIES OF RARICIRRUS (POLYCHAETA, CTENODRILIDAE) FROM THE CONTINENTAL SLOPE OF THE LAPTEV SEA NEAR THE GAKKEL RIDGE G.N. Buzhinskaja 1 * and R.V. Smirnov 2 1, 2 Zoological Institute of the Russian Academy of Sciences, Universitetskaya Emb. 1, Saint Petersburg, Russia; Galina.Buzhinskaja@zin.ru, Roman.Smirnov@zin.ru, vsroman@inbox.ru ABSTRACT Raricirrus arcticus sp. nov. is described with specimens collected near the Gakkel Ridge, Laptev Sea, from one station in the hydrothermal area, at nearly 2000 m. The new species differs from the other species of the genus in the presence of long serrate chaetae with thin straight tips in neuropodia of the middle part of the body, and in the position of the heart body, which first appears much more anteriorly than in all previously described species of both genera comprising the subfamily Raphidrilinae Hartmann-Schröder, Raricirrus arcticus sp. nov. is likely most closely related to the geographically nearest R. beryli Petersen et George, 1991 sharing the absence of a modified region with enlarged spines and the presence of distinct ventral ciliary fields in the area of the mouth and the neural ciliary band on a few anterior segments. Asexual and sexual reproduction is noted for the new species. The hypothesis of Petersen and George (1991) about the role of the heart body in the head regeneration process is supported by revealed correlation of the anteriormost occurrence of the heart body with the number of segments in anterior regenerates in R. arcticus sp. nov., as in other Raricirrus species. Systematic position of the family Ctenodrilidae and taxonomic differences between the genera Raricirrus Hartman, 1961 and Raphidrilus Monticelli, 1910 are discussed. Morphological characters useful in distinguishing species within the genus Raricirrus are defined. A key to identify the known species of Raricirrus is given. Key words: Arctic Ocean, Ctenodrilidae, morphology, Polychaeta, Raricirrus arcticus sp. nov., reproduction НОВЫЙ ВИД RARICIRRUS (POLYCHAETA, CTENODRILIDAE) С КОНТИНЕНТАЛЬНОГО СКЛОНА МОРЯ ЛАПТЕВЫХ В РАЙОНЕ ХРЕБТА ГAККЕЛЯ Г.Н. Бужинская 1 * и Р.В. Смирнов 2 1, 2 Зоологический институт Российской академии наук, Университетская наб. 1, Санкт-Петербург, Россия; Galina.Buzhinskaja@zin.ru, Roman.Smirnov@zin.ru, vsroman@inbox.ru РЕЗЮМЕ Приводится описание нового вида рода Raricirrus Hartman, 1961, найденного на глубине около 2000 м в море Лаптевых. Экземпляры Raricirrus arcticus sp. nov. были добыты в гидротермальном районе в зоне разлома, отделяющего хребет Гаккеля от Бассейна Нансена. Новый вид отличается от других видов рода наличием длинных зазубренных щетинок с тонкими прямыми концами в нейроподиях средней части тела и положением сердечного тела, которое начинается значительно ближе к голове, чем у всех видов, ранее описанных в обоих родах, составляющих подсемейство Raphidrilinae Hartmann-Schröder, Rariccirrus arcticus sp. nov. вероятно наиболее близкородственен географически ближайшему R. beryli Petersen et George, Оба вида объединяет отсутствие модифицированного отдела тела с увеличенными крючками и наличие отчетливых *Corresponding author / Автор-корреспондент
2 426 G.N. Buzhinskaja and R.V. Smirnov ресничных полей на вентральной стороне тела в области ротового отверстия и нейральной ресничной полоски на нескольких передних сегментах тела. У нового вида обнаружено бесполое и половое размножение. Выявлена корреляция между передним положением сердечного тела и количеством сегментов в головных регенератах R. arcticus sp. nov. и других видах рода Raricirrus, что поддерживает гипотезу M. Петерсен и Д. Джорджa (Petersen and George 1991) о роли сердечного тела в процессе регенерации головы у представителей рода. Обсуждаются систематическое положение семейства Ctenodrilidae и таксономические различия между родами Raricirrus и Raphidrilus Monticelli, Определены морфологические признаки, пригодные для различения видов в пределах рода Raricirrus. Представлен определительный ключ для известных видов Raricirrus. Ключевые слова: Северный Ледовитый океан, Ctenodrilidae, морфология, Polychaeta, Raricirrus arcticus sp. nov., размножение INTRODUCTION The collection gathered during the expedition of the German research vessel Polarstern in the Arctic Ocean in 1993 contained the first specimens of ctenodrilid polychaetes to be reported from Eurasian Arctic Seas. The worms were obtained from the Laptev Sea and initially were recorded as Raricirrus sp. without description (Buzhinskaja 2001). In the present paper the specimens are described as Raricirrus arcticus, new species of the subfamily Raphidrilinae Hartmann-Schröder, Only three species of the genus Raricirrus Hartman, 1961 were hitherto described: R. maculatus Hartman, 1961 from the northeastern Pacific off California, R. beryli Petersen et George, 1991 from the north-eastern Atlantic, and R. variabilis Dean, 1995 from the Caribbean. Among these species only R. variabilis was found living in deep-water, 4000 m depth, while the two other species are known from shallow waters at depths ranging from 46 to 300 m. Raricirrus maculatus and R. beryli possess both sexual and asexual modes of reproduction, and only sexual reproduction is known for R. variabilis (Dean 1995). The material herein reported allowed us to study reproductive patterns of R. arcticus sp. nov. The subfamily Raphidrilinae Hartmann-Schröder, 1971 comprises two genera: Raphidrilus Monticelli, 1910 and Raricirrus (Petersen and George 1986). This paper provides additional evidence concerning the taxonomic separation of these genera, and further elucidates their diagnostic characters. The systematic position of the family Ctenodrilidae is briefly discussed and it is retained as a separate family from Cirratulidae. Institutional abbreviations. ZIN: Zoological Institute, Russian Academy of Sciences (Saint Petersburg), Russia. MATERIAL AND METHODS A few dozen specimens of ctenodrilid-like polychaetes were taken by Agassiz trawl from m depth along the continental slope in the northern Laptev Sea, in the fault zone separating the Gakkel Ridge from the Nansen Basin. This fault zone is seismically and thermally active (Kim et al. 2006). The specimens of Raricirrus arcticus sp. nov. were found on the surface sediment layer among subfossil bivalve shells belonging to the genus Archivesica Dall, 1908 (fam. Vesicomyidae). These mussels are characteristic inhabitants of cold seeps and hydrothermal vents, and the presence of their shells indicates that the actual seeping activity in the neighborhood of the Gakkel Ridge is low or absent now, though methane and hydrogen sulfide are still detected in the sediments (Sirenko et al. 2004; Kim at al. 2006). Any representatives of infauna were absent in the sample (Kim at al. 2006). The sediments were mainly mud with clay. The material was originally fixed in 75% ethanol or 4% formaldehyde and later transferred to alcohol. Specimens were studied using both light microscopy and scanning electron microscopy (SEM). SEM photos were taken by Quanta 250 after specimens had been critical-point dried and coated with platinum. The observations, measurements and drawings were performed using standard binocular and compound light microscopes with a camera lucida. All material is deposited at the Zoological Institute of the Russian Academy of Sciences, Saint Petersburg (ZIRAS).
3 Raricirrus arcticus sp. nov. 427 SYSTEMATICS Family Ctenodrilidae Kennel, 1882 Subfamily Raphidrilinae Hartmann-Schröder, 1971 Genus Raricirrus Hartman, 1961 Raricirrus arcticus sp. nov. (Figs. 1 3) Raricirrus sp. Buzhinskaja 2001: 59. Material examined. R.V. Polarstern, , ARK-IX/4 (expedition), station 50: North of the Laptev Sea, N, E, depth m, bottom silty pelite with a strong odour of hydrogen sulfide and some part of fine sand, temperature near bottom 0.81 C, salinity Gear: AGT (Agassiz trawl). Collected by B.I. Sirenko. Type material: holotype ZIRAS 1/50650; paratypes ZIRAS 2/50561 (25 specimens). Etymology. The specific name refers to the occurrence of the species in the Arctic Ocean. Description Tube. Tubes consist of pellicle with dense layer of small grey or rust-coloured particles (grains of sand and silt) agglutinated together by mucus; upper layer weaker, more delicate. Two or rarely three specimens occur in same tube laying tightly side by side head to tail. A few adherent tubes found. Body. Holotype (Fig. 1A) 14.5 mm long, 0.75 mm maximum width (widest segment in midbody part), 30 chaetigers; last 9 chaetigers narrower, forming a slightly depressed caudal region. Paratypes up to 35 segments and about 20 mm in length, with up to 12 (usually 8 10) chaetigers in caudal region. Prostomium oval-triangular, with lateral oral folds; eyes lacking. Nuchal organs not clearly discernible among wide patches of cilia along anterolateral surfaces of the head (Fig. 2A). Ciliary fields also present anterior and posterior to the mouth and as a narrow ventral band on first few (up to five) chaetigers (Fig. 2B, C). Prostomium, peristomium and first chaetiger continuous dorsally, separated ventrally. Branchiae long, filiform, emerging posterodorsal to notochaetae, near posterior border of segments, very fragile and easily lost or broken (Fig. 2B, D). Holotype has complete branchiae on chaetiger 11 and underdeveloped one on chaetiger 12. A few pairs of branchiae in paratypes are located on variable chaetigers, such as 5 9, 6 8, 9 11, 10 12, and one pair on the 13. Pygidium oval-triangular with dorsoterminal anus (Fig. 2E). Heart body in dorsal blood vessel, clearly visible as pink tube beginning in second chaetiger, convoluted and thickened along chaetigers (Fig. 1A). All paratypes have heart body pink to brown (black from chaetigers 12 14), extending from chaetiger two to chaetigers depending on worm size, convoluted (staggered) beginning from 3 13 chaetiger in different specimens and slightly widened on midbody segments (6 10, 7 9 or 9 13). Noto- and neurochaetal bundles emerging directly from body wall, lateral in anterior segments, displaced more ventrolaterally posteriorly (Fig. 2F). Notochaetae of two types: 4 12 capillaries (1 4 longer and 3 8 shorter ones in each anterior and midbody bundle), tips finely serrate, and 2 3 straight thick, coarsely serrate chaetae in caudal region. Capillaries on chaetigers 3 11 longer than body width. Neurochaetae of three types: 3 9 pectinate falcigers anteriorly with 1 3 longer serrate chaetae with thin straight smooth tips in midbody chaetigers, and posteriorly 1 2 coarsely serrate chaetae similar to those found in caudal notopodia. Pectinate falcigers short or long with different size of teeth in different chaetae (Figs. 2G, I, J, 3A, B). Long serrate chaetae with triangular teeth decreasing gradually in size towards chaetal tips (Figs. 2I, 3C, D). Coarsely serrate chaetae with different forms of teeth, including some forked teeth (Fig. 2H, K, L). No modified segments. Heavy spines in chaetal bundles absent (Fig. 2E). Few oocytes observed in 10 segments (in chaetigers 7 16) of one specimen having 30 chaetigers. Oocytes oval, μm in max diameter, or rounded with up to 36 μm in diameter. Only one short fragment of midbody region of probably dispersal (epitokous) stage found, with longer, abundant capillary chaetae in notopodial bundles. Juvenile specimen 1.9 mm long, 0.27 mm wide (in widest region) with 15 chaetigers and five achaetous underdeveloped segments (Fig. 1B). Heart body convoluted, extending through three segments in chaetigers 2 4. One pair of short branchiae on chaetiger 7, and one branchia on chaetiger 11. Most of specimens in different stages of regeneration of either anterior or posterior ends (Fig. 1C), or in both of them (Fig. 1D, E). In anterior region no more than 1 2 regenerated segments, while in posterior region regenerates consist of much more numerous segments.
4 428 G.N. Buzhinskaja and R.V. Smirnov Fig. 1. Raricirrus arcticus sp. nov. A holotype, dorsal view of anterior region; heart body visible from chaetiger two; branchiae present on chaetigers 11 and 12; B juvenile specimen; heart body begins from chaetiger two; branchiae present full-size on chaetiger 7 and as buds on chaetiger 11; C specimen regenerating anterior end; D, E specimens regenerating both anterior and posterior ends. Colour of worms red-brown. Head and anterior segments often with red spots. Remarks. Raricirrus arcticus sp. nov. differs from other species of the genus in the position of the heart body, which first appears much more anteriorly, in chaetiger 2, and also in the presence of long serrate chaetae with thin straight tips in neuropodia of the midbody region. The anteriormost occurrence of the heart body is likely correlated in R. arcticus sp. nov., as in other Raricirrus species, with the number of segments in anterior regenerates, which confirms the idea of Petersen and George (1991) about the role of the heart body in the regeneration of anterior region in this genus. Raricirrus arcticus sp. nov.
5 Raricirrus arcticus sp. nov. 429 Fig. 2. Raricirrus arcticus sp. nov. SEM photos. A dorsolateral view of anterior end showing continuous ciliary patches without clearly differentiated nuchal organs; B anterior region of whole specimen in mainly ventral view showing ventral ciliation in front of and posterior to mouth, continuing as a ventral band, anteriorly wide, then gradually narrowing and finally vanished on segment five; branchiae is visible in midbody region; C anterior end, ventral view, showing wide ciliary fields in mouth area; D two branchiae showing absence of club-like ends; E posterior region, ventral view; F right side of an anterior chaetiger showing notopodial capillaries long or short, and regular neuropodial pectinate falcigers; G midbody neuropodial pectinate falcigers and long serrate chaetae with thin straight tips; H tip of coarsely serrate neurochaeta; I details of tips of pectinate falciger and of long serrate neurochaetae; J detail of tips of neuropodial short pectinate falcigers; K bundle of posterior notochaetae with long slender capillaries and stout coarsely serrate chaetae; L neuropodium of posterior region with pectinate falcigers and coarsely serrate chaetae.
6 430 G.N. Buzhinskaja and R.V. Smirnov Raricirrus arcticus sp. nov. differs from R. beryli in the structure of nuchal organs, which cannot be differentiated from wide patches of cilia on the dorsolateral sides of the prostomium. Probably similar nuchal organs are described in R. maculatus, but photo is absent (Hartman 1961; Petersen and George 1991). Thus, the following morphological characters are useful in distinguishing species within the genus Raricirrus: 1) Position of the heart body; 2) Presence or absence of notopodial pectinate falcigers; 3) Presence or absence of long serrate chaetae with thin straight tips in neuropodia; 4) Presence or absence of a modified region with large hooked spines; 5) Number of segments in the modified region; 6) Presence/ development of ciliary patches on the prostomium and peristomium, and ventral ciliary band on anterior segments; 7) Structure of the nuchal organs; 8) Structure of the branchiae; 9) Presence or absence of an asexual reproductive mode; 10) Relative length of capillaries in epitokous worms. Distribution. Laptev Sea, Arctic Ocean ( m depth). Key to the species of the genus Raricirrus Fig. 3. Raricirrus arcticus sp. nov. A, B short and long pectinate falcigers; C, D long serrate neurochaetae with thin straight tips. demonstrates great morphological similarity with the geographically nearest R. beryli. These species are likely most closely related sharing the absence of a modified region with enlarged spines and the presence of distinct ventral ciliary fields in the area of the mouth and the neural ciliary band on a few anterior segments. The new species resembles R. beryli and R. maculatus in the possession of uniform filamentous branchiae, asexual reproductive mode, and the absence of notopodial pectinate falcigers. Raricirrus variabilis appears to be unique among the congeners in the absence of asexual reproduction, the presence of branchiae with club-like ends, pectinate falcigers in notopodia, and the presence of reproductive stylet and a seminal vesicle. 1a. Branchiae with clublike ends. Pectinate falcigers in notopodia. Only sexual reproductive mode... R. variabilis 1b. Branchiae cylindrical. No pectinate falcigers in notopodia. Sexual and asexual reproduction a. Distinct ventral ciliary fields near mouth and neural ciliary band on a few anterior segments. No modified region with enlarged spines b. Ventral ciliation absent, or not clearly discernible. Modified region with large hooked spines in some specimens R. maculatus 3a. Heart body begins from chaetiger 2. Nuchal organs inconspicuous among anterolateral patches of cilia R. arcticus 3b. Heart body begins from chaetigers Nuchal organs areas without cilia, surrounded by ciliary fields R. beryli DISCUSSION The new species undoubtedly belongs to the family Ctenodrilidae, though the differentiation of Ctenodrilidae and Cirratulidae is uncertain. The ctenodrilids have an evident resemblance with cirratulids, but differs from them by absence of grooved tentacles. Thus, it is possible to take some
7 Raricirrus arcticus sp. nov. 431 juvenile cirratulids (still without the tentacles) for ctenodrilids. Hartmann-Schröder (1971, 1996) and Magalhães et al. (2011) treated them as distinct in the morphological studies, and Salazar-Vallejo et al. (2008) in a restricted phylogenetic analysis considered the family Ctenodrilidae monophyletic, but at least some molecular studies placed them within cirratulids (e.g. Rousset et al. 2007). Weidhase et al. (2016) further reported that Raricirrus and Ctenodrilus species were nested within Cirratulidae, with R. beryli as a sister taxon to a clade comprising the multi-tentaculate cirratulid genera. The molecular data might reflect the classification of the Ctenodrilidae in two subfamilies by Petersen and George (1991): Ctenodrilinae, including Ctenodrilus serratus (Schmidt, 1857), and Raphidrilinae, including R. beryli, rather than support the monophyly of the family Ctenodrilidae. Also stout serrated chaetae found in all ctenodrilid species, including the new species described here, imply the possibility of progenetic evolution: these chaetae are similar to those in juveniles of cirratulids (Weidhase et al. 2016). Additionally, in the ontogeny of some multitentaculate cirratulids, the branchiae, which are also present in Raricirrus and Raphidrilus, are developed prior to the tentacles (Claparède and Mecznikow 1869; Wilson 1936; Okuda 1946). Given the close relationship of Raricirrus to multitentaculate cirratulids and the hypothesized progenetic evolution of this taxon, Weidhase et al. (2016) suggested that the absence of tentacles represents a juvenile character. Furthermore, the two genera of ctenodrilids with branchiae and long bodies, Raricirrus and Raphidrilus comprising the subfamily Raphidrilinae, are initially very morphologically close and have many overlapping features. Nevertheless, the genera were confirmed to be distinct by Petersen and George (1991) based on the position of the heart body, the structure of the nuchal organs and the head region. Dean (1995) considered the first two features to be a species level based on variability among species of Raricirrus, and suggested that the distinctness between Raricirrus and Raphidrilus are due to the chaetal characteristics and the head structure. Magalhães et al. (2011) further elucidated the diagnostic features of Raphidrilus, and reported the presence of at least one dorsally biannulated achaetous segment between the peristomium and first chaetiger, and an indistinct posterior region in all Raphidrilus species, thus confirming that the two genera are close but not identical. The present study of R. arcticus sp. nov. reveals the occurrence of the heart body most anterior among all previously described species of both Raricirrus and Raphidrilus, which confirms the species level value of this character. In addition, the indistinct nuchal organs in R. arcticus sp. nov., possibly similar to those of R. maculatus, but unlike the nuchal organs of other ctenodrilids, imply the great variability of this character within the genus Raricirrus, while the structure of the head and caudal region, and the arrangement of the chaetae are indeed useful for distinguishing Raricirrus and Raphidrilus. ACKNOWLEDGEMENTS We thank the crew and scientific staff of the research vessel Polarstern (cruise ARK-IX/4, 1993) for the opportunity to report the ctenodrilids for the first time from the deep Arctic Basin. Our special thanks are due to Dr. Boris Sirenko (Zoological Institute RAS, Saint Petersburg) for lending us the material and his support. We are also very grateful to Dr. Sergio Salazar-Vallejo for valuable remarks to the manuscript and his attention to our study. The work was carried out using the equipment of the Taxon Research Resource Center ( ckp/3038/?sphrase_id= ) and the research collections of the Zoological Institute RAS (Saint Petersburg). REFERENCES Buzhinskaja G.N Class Polychaeta. In: List of species of free living invertebrates of Eurasian Arctic seas and adjacent deep waters. Explorations of the fauna of the seas, 51(59): Claparède E. and Mecznikow E Beiträge zur Kenntnis der Entwicklungsgeschichte der Chaetopoden. Zeitschrift für wissenschaftliche Zoologie, 19: Dean H.K A new species of Raricirrus (Polychaeta: Ctenodrilidae) from wood collected in the Tongue of the Ocean, Virgin Islands. Proceedings of the Biological Society of Washington, 108: Hartman O Polychaetous annelids from California. Allan Hancock Pacific Expeditions, 25: Hartmann-Schröder G Annelida, Borstenwürmer, Polychaeta. Die Tierwelt Deutschlands und der angrenzenden Meeresteile nach ihren Merkmalen und nach ihrer Lebensweise. Gustav Fischer Verlag, Jena, 58: 594. Hartmann-Schröder G Annelida, Borstenwürmer, Polychaeta. 2., neubearb. Aufl. Die Tierwelt Deutschlands und der angrenzenden Meeresteile nach ihren Merkmalen und nach ihrer Lebensweise. Gustav Fischer Verlag, Jena, 58: 648 p.
8 432 G.N. Buzhinskaja and R.V. Smirnov Kim B., Rachor E., Sirenko B., Aplonov V., Starobogatov Ya. and Stein R Thermal discharge points on the Gakkel Ridge (Arctic Basin). Explorations of the fauna of the seas, 56(64): Magalhães W.F., Bailey-Brock J.H. and Davenport J.S On the genus Raphidrilus Monticelli, 1910 (Polychaeta: Ctenodrilidae) with description of two new species. Zootaxa, 2804: Okuda Sh Studies on the development of Annelida Polychaeta. Journal of the Faculty of Science, Hokkaido Imperial University, series VI, 9(2): Petersen M.E. and George J.D A new species of Raricirrus from Northern Europe, with notes on its biology and a discussion of the affinities of the genus (Polychaeta: Ctenodrilidae). Ophelia Supplement, 5: Rousset V., Pleijel F., Rouse G.W., Erséus C. and Siddall M.E A molecular phylogeny of annelids. Cladistics, 23: Salazar-Vallejo S.I., Carrera-Parra L.F. and Fauchald K Phylogenetic affinities of the Flabelligeridae (Annelida, Polychaeta). Journal of Zoological Systema tics and Evolutionary Research, 46(3): Sirenko B., Denisenko S., Deubel H. and Rachor E Deep water communities of the Laptev Sea and adjacent parts of Arctic Ocean. Explorations of the fauna of the seas, 54(62): Weidhase M., Bleidorn C. and Simon C.A On the taxonomy and phylogeny of Ctenodrilus (Annelida: Cirratulidae) with a first report from South Africa. Marine Biodiversity, 46(1): Wilson D.P The development of Audouinia tentaculata (Montagu). Journal of Marine Biological Association of the United Kingdom, 20: Submitted 12 July 2017; accepted November 13, 2017.
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